Abstract
Although a growing number of studies have investigated the neural mechanisms of reinforcement learning, it remains unclear how the brain responds to feedback that is unreliable. A recent theory proposes that the reward positivity (RewP) component of the event-related brain potential (ERP) and frontal midline theta (FMT) power reflect separate feedback-related processing functions of anterior cingulate cortex (ACC). In the present study, the electroencephalogram (EEG) was recorded from participants as they engaged in a time estimation task in which feedback reliability was manipulated across conditions. After each response, they received a cue that indicated that the following feedback stimulus was 100%, 75%, or 50% reliable. The results showed that participants' time estimates adjusted linearly according to the feedback reliability. Moreover, presentation of the cue indicating 100% reliability elicited a larger RewP-like ERP component than the other cues did, and feedback presentation elicited a RewP of approximately equal amplitude for all of the three reliability conditions. By contrast, FMT power elicited by negative feedback decreased linearly from the 100% condition to 75% and 50% condition, and only FMT power predicted behavioral adjustments on the following trials. In addition, an analysis of Beta power and cross-frequency coupling (CFC) of Beta power with FMT phase suggested that Beta-FMT communication modulated motor areas for the purpose of adjusting behavior. We interpreted these findings in terms of the hierarchical reinforcement learning account of ACC, in which the RewP and FMT are proposed to reflect reward processing and control functions of ACC, respectively.
Highlights
Adaptive decision making depends on a network of neural systems for cognitive control that includes the anterior cingulate cortex (ACC), a brain area believed to contribute to multipleElectronic supplementary material The online version of this article contains supplementary material, which is available to authorized users.Cogn Affect Behav Neurosci (2018) 18:949–963 exactly how the ACC utilizes these reward signals to regulate behavior remains unclear (Holroyd & Umemoto, 2016; Umemoto, HajiHosseini, Yates & Holroyd, 2017). feedback processing by ACC has been studied extensively, relatively few studies have examined the effect of unreliable or uncertain feedback on ACC
We examined the reward positivity (RewP), frontal midline theta (FMT), and Beta power to elucidate how ACC processes reliable versus unreliable reward information to regulate behavior
We found that coupling of FMT phase with Beta power was associated with behavioral adjustments on the following trial
Summary
As noted numerous human electrophysiological studies have examined feedback processing by ACC (for reviews, see Sambrook & Goslin, 2015; Walsh & Anderson, 2012), only a few of these studies investigated how reliability modulates feedback processing (Ernst & Steinhauser, 2015; Ernst & Steinhauser, 2017; Schiffer, Siletti, Waszak, & Yeung, 2017). These studies examined the electrophysiological effects of feedback processing only in the time domain, i.e., using the event-related brain potential (ERP), and reported inconsistent results. Most of these studies only tested two feedback conditions (reliable or not), leaving unresolved the question of whether the ACC control signal scales parametrically with feedback reliability
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